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Solute Carrier Transporters as Potential Targets for the Treatment of Metabolic Disease

Tina Schumann, Jörg König, Christine Henke, Diana M. Willmes, Stefan R. Bornstein, Jens Jordan, Martin F. Fromm and Andreas L. Birkenfeld
Martin C. Michel, ASSOCIATE EDITOR
Pharmacological Reviews January 2020, 72 (1) 343-379; DOI: https://doi.org/10.1124/pr.118.015735
Tina Schumann
Section of Metabolic and Vascular Medicine, Medical Clinic III, Dresden University School of Medicine (T.S., C.H., D.M.W., S.R.B.), and Paul Langerhans Institute Dresden of the Helmholtz Center Munich at University Hospital and Faculty of Medicine (T.S., C.H., D.M.W.), Technische Universität Dresden, Dresden, Germany; Deutsches Zentrum für Diabetesforschung e.V., Neuherberg, Germany (T.S., C.H., D.M.W., A.L.B.); Clinical Pharmacology and Clinical Toxicology, Institute of Experimental and Clinical Pharmacology and Toxicology, Friedrich-Alexander-Universität Erlangen-Nürnberg, Erlangen, Germany (J.K., M.F.F.); Institute for Aerospace Medicine, German Aerospace Center and Chair for Aerospace Medicine, University of Cologne, Cologne, Germany (J.J.); Diabetes and Nutritional Sciences, King’s College London, London, United Kingdom (S.R.B., A.L.B.); Institute for Diabetes Research and Metabolic Diseases of the Helmholtz Centre Munich at the University of Tübingen, Tübingen, Germany (A.L.B.); and Department of Internal Medicine, Division of Endocrinology, Diabetology and Nephrology, Eberhard Karls University Tübingen, Tübingen, Germany (A.L.B.)
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Jörg König
Section of Metabolic and Vascular Medicine, Medical Clinic III, Dresden University School of Medicine (T.S., C.H., D.M.W., S.R.B.), and Paul Langerhans Institute Dresden of the Helmholtz Center Munich at University Hospital and Faculty of Medicine (T.S., C.H., D.M.W.), Technische Universität Dresden, Dresden, Germany; Deutsches Zentrum für Diabetesforschung e.V., Neuherberg, Germany (T.S., C.H., D.M.W., A.L.B.); Clinical Pharmacology and Clinical Toxicology, Institute of Experimental and Clinical Pharmacology and Toxicology, Friedrich-Alexander-Universität Erlangen-Nürnberg, Erlangen, Germany (J.K., M.F.F.); Institute for Aerospace Medicine, German Aerospace Center and Chair for Aerospace Medicine, University of Cologne, Cologne, Germany (J.J.); Diabetes and Nutritional Sciences, King’s College London, London, United Kingdom (S.R.B., A.L.B.); Institute for Diabetes Research and Metabolic Diseases of the Helmholtz Centre Munich at the University of Tübingen, Tübingen, Germany (A.L.B.); and Department of Internal Medicine, Division of Endocrinology, Diabetology and Nephrology, Eberhard Karls University Tübingen, Tübingen, Germany (A.L.B.)
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Christine Henke
Section of Metabolic and Vascular Medicine, Medical Clinic III, Dresden University School of Medicine (T.S., C.H., D.M.W., S.R.B.), and Paul Langerhans Institute Dresden of the Helmholtz Center Munich at University Hospital and Faculty of Medicine (T.S., C.H., D.M.W.), Technische Universität Dresden, Dresden, Germany; Deutsches Zentrum für Diabetesforschung e.V., Neuherberg, Germany (T.S., C.H., D.M.W., A.L.B.); Clinical Pharmacology and Clinical Toxicology, Institute of Experimental and Clinical Pharmacology and Toxicology, Friedrich-Alexander-Universität Erlangen-Nürnberg, Erlangen, Germany (J.K., M.F.F.); Institute for Aerospace Medicine, German Aerospace Center and Chair for Aerospace Medicine, University of Cologne, Cologne, Germany (J.J.); Diabetes and Nutritional Sciences, King’s College London, London, United Kingdom (S.R.B., A.L.B.); Institute for Diabetes Research and Metabolic Diseases of the Helmholtz Centre Munich at the University of Tübingen, Tübingen, Germany (A.L.B.); and Department of Internal Medicine, Division of Endocrinology, Diabetology and Nephrology, Eberhard Karls University Tübingen, Tübingen, Germany (A.L.B.)
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Diana M. Willmes
Section of Metabolic and Vascular Medicine, Medical Clinic III, Dresden University School of Medicine (T.S., C.H., D.M.W., S.R.B.), and Paul Langerhans Institute Dresden of the Helmholtz Center Munich at University Hospital and Faculty of Medicine (T.S., C.H., D.M.W.), Technische Universität Dresden, Dresden, Germany; Deutsches Zentrum für Diabetesforschung e.V., Neuherberg, Germany (T.S., C.H., D.M.W., A.L.B.); Clinical Pharmacology and Clinical Toxicology, Institute of Experimental and Clinical Pharmacology and Toxicology, Friedrich-Alexander-Universität Erlangen-Nürnberg, Erlangen, Germany (J.K., M.F.F.); Institute for Aerospace Medicine, German Aerospace Center and Chair for Aerospace Medicine, University of Cologne, Cologne, Germany (J.J.); Diabetes and Nutritional Sciences, King’s College London, London, United Kingdom (S.R.B., A.L.B.); Institute for Diabetes Research and Metabolic Diseases of the Helmholtz Centre Munich at the University of Tübingen, Tübingen, Germany (A.L.B.); and Department of Internal Medicine, Division of Endocrinology, Diabetology and Nephrology, Eberhard Karls University Tübingen, Tübingen, Germany (A.L.B.)
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Stefan R. Bornstein
Section of Metabolic and Vascular Medicine, Medical Clinic III, Dresden University School of Medicine (T.S., C.H., D.M.W., S.R.B.), and Paul Langerhans Institute Dresden of the Helmholtz Center Munich at University Hospital and Faculty of Medicine (T.S., C.H., D.M.W.), Technische Universität Dresden, Dresden, Germany; Deutsches Zentrum für Diabetesforschung e.V., Neuherberg, Germany (T.S., C.H., D.M.W., A.L.B.); Clinical Pharmacology and Clinical Toxicology, Institute of Experimental and Clinical Pharmacology and Toxicology, Friedrich-Alexander-Universität Erlangen-Nürnberg, Erlangen, Germany (J.K., M.F.F.); Institute for Aerospace Medicine, German Aerospace Center and Chair for Aerospace Medicine, University of Cologne, Cologne, Germany (J.J.); Diabetes and Nutritional Sciences, King’s College London, London, United Kingdom (S.R.B., A.L.B.); Institute for Diabetes Research and Metabolic Diseases of the Helmholtz Centre Munich at the University of Tübingen, Tübingen, Germany (A.L.B.); and Department of Internal Medicine, Division of Endocrinology, Diabetology and Nephrology, Eberhard Karls University Tübingen, Tübingen, Germany (A.L.B.)
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Jens Jordan
Section of Metabolic and Vascular Medicine, Medical Clinic III, Dresden University School of Medicine (T.S., C.H., D.M.W., S.R.B.), and Paul Langerhans Institute Dresden of the Helmholtz Center Munich at University Hospital and Faculty of Medicine (T.S., C.H., D.M.W.), Technische Universität Dresden, Dresden, Germany; Deutsches Zentrum für Diabetesforschung e.V., Neuherberg, Germany (T.S., C.H., D.M.W., A.L.B.); Clinical Pharmacology and Clinical Toxicology, Institute of Experimental and Clinical Pharmacology and Toxicology, Friedrich-Alexander-Universität Erlangen-Nürnberg, Erlangen, Germany (J.K., M.F.F.); Institute for Aerospace Medicine, German Aerospace Center and Chair for Aerospace Medicine, University of Cologne, Cologne, Germany (J.J.); Diabetes and Nutritional Sciences, King’s College London, London, United Kingdom (S.R.B., A.L.B.); Institute for Diabetes Research and Metabolic Diseases of the Helmholtz Centre Munich at the University of Tübingen, Tübingen, Germany (A.L.B.); and Department of Internal Medicine, Division of Endocrinology, Diabetology and Nephrology, Eberhard Karls University Tübingen, Tübingen, Germany (A.L.B.)
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Martin F. Fromm
Section of Metabolic and Vascular Medicine, Medical Clinic III, Dresden University School of Medicine (T.S., C.H., D.M.W., S.R.B.), and Paul Langerhans Institute Dresden of the Helmholtz Center Munich at University Hospital and Faculty of Medicine (T.S., C.H., D.M.W.), Technische Universität Dresden, Dresden, Germany; Deutsches Zentrum für Diabetesforschung e.V., Neuherberg, Germany (T.S., C.H., D.M.W., A.L.B.); Clinical Pharmacology and Clinical Toxicology, Institute of Experimental and Clinical Pharmacology and Toxicology, Friedrich-Alexander-Universität Erlangen-Nürnberg, Erlangen, Germany (J.K., M.F.F.); Institute for Aerospace Medicine, German Aerospace Center and Chair for Aerospace Medicine, University of Cologne, Cologne, Germany (J.J.); Diabetes and Nutritional Sciences, King’s College London, London, United Kingdom (S.R.B., A.L.B.); Institute for Diabetes Research and Metabolic Diseases of the Helmholtz Centre Munich at the University of Tübingen, Tübingen, Germany (A.L.B.); and Department of Internal Medicine, Division of Endocrinology, Diabetology and Nephrology, Eberhard Karls University Tübingen, Tübingen, Germany (A.L.B.)
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Andreas L. Birkenfeld
Section of Metabolic and Vascular Medicine, Medical Clinic III, Dresden University School of Medicine (T.S., C.H., D.M.W., S.R.B.), and Paul Langerhans Institute Dresden of the Helmholtz Center Munich at University Hospital and Faculty of Medicine (T.S., C.H., D.M.W.), Technische Universität Dresden, Dresden, Germany; Deutsches Zentrum für Diabetesforschung e.V., Neuherberg, Germany (T.S., C.H., D.M.W., A.L.B.); Clinical Pharmacology and Clinical Toxicology, Institute of Experimental and Clinical Pharmacology and Toxicology, Friedrich-Alexander-Universität Erlangen-Nürnberg, Erlangen, Germany (J.K., M.F.F.); Institute for Aerospace Medicine, German Aerospace Center and Chair for Aerospace Medicine, University of Cologne, Cologne, Germany (J.J.); Diabetes and Nutritional Sciences, King’s College London, London, United Kingdom (S.R.B., A.L.B.); Institute for Diabetes Research and Metabolic Diseases of the Helmholtz Centre Munich at the University of Tübingen, Tübingen, Germany (A.L.B.); and Department of Internal Medicine, Division of Endocrinology, Diabetology and Nephrology, Eberhard Karls University Tübingen, Tübingen, Germany (A.L.B.)
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Martin C. Michel
Roles: ASSOCIATE EDITOR
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    Fig. 1.

    Cellular localization of potential SLC targets for the treatment of metabolic disease. SLC transporters are expressed in the plasma membrane or intracellular membranes. Of the five presented SLC families, which are displayed in different colors, 13 members have been assessed to exhibit strong evidence of association with metabolic disease based on human studies and mouse models. The equal shapes of the transporter symbols do not correspond to the different modes of transport, but the arrows indicate transport direction, for example, whether the transporter is proposed to mediate influx of its substrates into the cell (SLC5A1, SLC5A2, SLC13A5) or intracellular compartments (SLC25A7, SLC25A8, SLC25A9, SLC30A8), facilitates both influx and efflux (SLC16A1, SLC16A11, SLC16A13), or acts as an exchanger (SLC25A13, SLC25A20, SLC25A24). The main substrates of the transporters are indicated next to the transporter symbol, except for SLC16A13, which is not characterized at all concerning substrate specificity and transport mode.

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    Fig. 2.

    Tissue distribution of potential SLC targets for the treatment of metabolic disease. SLC transporters are broadly expressed. The 13 SLCs, which belong to five families displayed in different colors and were evaluated to have strong potential as targets for the treatment of metabolic disease, are highly expressed in metabolically active organs such as the liver, kidney, brain, and intestine.

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    TABLE 1

    Potential SLC targets for the treatment of metabolic disease with strong evidence based on human studies and mouse models

    SLC NameProtein NameSubstratesExpression in Metabolically Active OrgansSubcellular LocalizationLink to Metabolic Disease in HumansLink to Metabolic Disease in MiceReferences
    SLC5A1SGLT1Glucose, galactoseKidney, intestinePlasma membraneGlucose/galactose malabsorptionGlucose/galactose malabsorption, impaired glucose toleranceTurk et al., 1991; Martin et al., 1996; Kasahara et al., 2001; Wright et al., 2011; Powell et al., 2013; Wright, 2013
    SLC5A2SGLT2GlucoseKidneyPlasma membraneFamilial glucosuriaObesity, insulin resistance, diabetesSanter et al., 2000, 2003; van den Heuvel et al., 2002; Jurczak et al., 2011; Wright et al., 2011; Powell et al., 2013; Wright, 2013
    SLC13A5NaCT, NaC2, INDYCitrate, succinate, malate, fumarateLiver, brain, adrenal glandsPlasma membraneObesity, NAFLDObesity, fatty liver, insulin resistanceBirkenfeld et al., 2011; Bergeron et al., 2013; Pesta et al., 2015; Brachs et al., 2016; von Loeffelholz et al., 2017b
    SLC16A1MCT1Lactate, pyruvate, ketone bodiesIntestine, heart, skeletal muscle, liver, kidney, adrenal glands, brain, adipose tissuePlasma membraneKetoacidosis, exercise- induced hyperinsulinemiaExercise-induced hyperinsulinemia, obesity, insulin resistance, hepatic steatosisHalestrap and Meredith, 2004; Otonkoski et al., 2007; Pullen et al., 2012; Lengacher et al., 2013; van Hasselt et al., 2014; Balasubramaniam et al., 2016; Carneiro et al., 2017
    SLC16A11MCT11PyruvateThyroid, liverEndoplasmic reticulum, plasma membraneT2DFatty liver, insulin resistance, diabetesWilliams et al., 2014; Lara-Riegos et al., 2015; Traurig et al., 2016; Rusu et al., 2017; Almeda-Valdes et al., 2019; Hidalgo et al., 2019; Zhao et al., 2019b
    SLC16A13MCT13UnknownLiver, kidney, intestineGolgi apparatusT2DN.A.Hara et al., 2014; Williams et al., 2014
    SLC25A7UCP1, thermogeninH+Brown adipose tissueInner mitochondrial membraneObesity, T2DObesityNicholls et al., 1978; Lowell et al., 1993; Kopecky et al., 1995; Kopecký et al., 1996a,b; Baumruk et al., 1999; Li et al., 2000; Palmieri, 2004; Gates et al., 2007; Brondani et al., 2012
    SLC25A8UCP2, UCPHH+Adipose tissue, skeletal muscle, liver, kidney, pancreas, heartInner mitochondrial membraneObesity, T2DObesityFleury et al., 1997; Gimeno et al., 1997; Arsenijevic et al., 2000; Zhang et al., 2001; Palmieri, 2013; Dalgaard, 2011
    SLC25A9UCP3H+Skeletal muscleInner mitochondrial membraneObesity, T2DObesityBoss et al., 1997; Lowell, 1999; Clapham et al., 2000; Gong et al., 2000; Vidal-Puig et al., 2000; Horvath et al., 2003; Jia et al., 2009; Palmieri, 2013
    SLC25A13AGC2, CTLN2, citrin aralar 2Aspartate, glutamateLiver, kidney, intestine, brain, pancreas, heart, skeletal muscle, adrenal glandsInner mitochondrial membraneNICCD, CTLN2CitrullinemiaKobayashi et al., 1999; Ohura et al., 2001; Tazawa et al., 2001; Sinasac et al., 2004; Saheki and Song, 2005; Takagi et al., 2006; Tsai et al., 2006; Saheki et al., 2007; Fukumoto et al., 2008; Komatsu et al., 2008; Chang et al., 2011; Palmieri, 2013; Hayasaka et al., 2018
    SLC25A20CAC, CACTCarnitine, acylcarnitineLiver, intestine, adrenal glands, heart, skeletal muscle, kidney, brain, pancreasInner mitochondrial membraneCarnitine carrier deficiencyN.A.Huizing et al., 1997; Indiveri et al., 2011; Palmieri, 2013
    SLC25A24APC1, MCSC1, SCAMC1Adenine nucleotides, phosphateIntestine, adipose tissue, adrenal glands, liver, pancreas, kidneyInner mitochondrial membraneObesityObesityPalmieri, 2013; Urano et al., 2015; Palmieri and Monne, 2016
    SLC30A8ZnT8ZincPancreasSecretory granuleT2DObesity, insulin resistanceChimienti et al., 2004; Saxena et al., 2007; Scott et al., 2007; Sladek et al., 2007; Boesgaard et al., 2008; Nicolson et al., 2009; Pound et al., 2009, 2012; Tamaki et al., 2009, 2013; Cauchi et al., 2010; Wijesekara et al., 2010; Kim et al., 2011; Flannick et al., 2014; Gerber et al., 2014; Shan et al., 2014; Maruthur et al., 2015; Rutter and Chimienti, 2015; Mitchell et al., 2016; Li et al., 2017a, 2018; Wong et al., 2017; Ding et al., 2018; Dong et al., 2018; Kleiner et al., 2018; Lin et al., 2018; Liu et al., 2018; Plengvidhya et al., 2018
    • View popup
    TABLE 2

    Potential SLC targets for the treatment of metabolic disease with limited evidence based on human studies or mouse models

    SLC NameProtein NameSubstratesExpression in Metabolically Active OrgansSubcellular LocalizationLink to Metabolic Disease in HumansLink to Metabolic Disease in MiceReferences
    SLC5A9SGLT4Mannose, glucose, fructoseIntestine, kidney, liverPlasma membraneDiabetic retinopathyN.A.Tazawa et al., 2005; Ung et al., 2017
    SLC5A10SGLT5Mannose, fructose, glucose, galactoseKidneyPlasma membraneN.A.Hepatic steatosisGrempler et al., 2012; Fukuzawa et al., 2013
    SLC13A1NaS1, NaSi-1Sulfate, thiosulfate, selenateKidney, intestine, adrenal glands, adipose tissuePlasma membraneDrug-induced hepatotoxicityFatty liverMarkovich, 2001; Dawson et al., 2006
    SLC13A2NaDC1, NaC1, SDCT1Succinate, α-ketoglutarate, citrateKidney, intestinePlasma membraneNephrolithiasisNephrolithiasisMarkovich and Murer, 2004; Ho et al., 2007; Bergeron et al., 2013; Udomsilp et al., 2018
    SLC13A3NaDC3, NaC3, SDCT2Succinate, α-ketoglutarate, citrateKidney, liver, brainPlasma membraneDiabetic nephropathy, chronic kidney diseaseN.A.Bento et al., 2008; Ju et al., 2009; Bergeron et al., 2013; Nanayakkara et al., 2014
    SLC16A3MCT4Lactate, pyruvate, ketone bodiesSkeletal muscle, brain, intestinePlasma membrane, nuclear membraneDiabetic nephropathyN.A.Lokman et al., 2011; Halestrap, 2013
    SLC16A9MCT9CarnitineKidney, adrenal glandsPlasma membraneGoutN.A.Kolz et al., 2009; van der Harst et al., 2010; Halestrap, 2013; Nakayama et al., 2013
    SLC16A10MCT10, TAT1Aromatic amino acidsSkeletal muscle, heart, kidney, intestine, pancreasPlasma membraneNAFLDN.A.Halestrap, 2013; Lake et al., 2015
    SLC25A25APC2, SCaMC-2, MCSCAdenine nucleotides, phosphateBrain, heart, skeletal muscle, liver, intestine, pancreasInner mitochondrial membraneN.A.ObesityAnunciado-Koza et al., 2011
    SLC25A40MCFPUnknownLiver, kidney, intestine, brain, adrenal glandsInner mitochondrial membraneHypertriglyceridemiaN.A.Rosenthal et al., 2013
    SLC30A3ZnT3ZincBrainSynaptic vesicleN.A.Impaired glucose tolerancePalmiter et al., 1996; Smidt et al., 2009; Keele et al., 2018
    SLC30A7ZnT7ZincIntestineGolgi apparatusN.A.Obesity, insulin resistanceKirschke and Huang, 2003; Huang et al., 2007, 2010, 2012, 2018
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Review ArticleReview Article

SLC Transporters as Targets to Treat Metabolic Disease

Tina Schumann, Jörg König, Christine Henke, Diana M. Willmes, Stefan R. Bornstein, Jens Jordan, Martin F. Fromm and Andreas L. Birkenfeld
Pharmacological Reviews January 1, 2020, 72 (1) 343-379; DOI: https://doi.org/10.1124/pr.118.015735

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SLC Transporters as Targets to Treat Metabolic Disease

Tina Schumann, Jörg König, Christine Henke, Diana M. Willmes, Stefan R. Bornstein, Jens Jordan, Martin F. Fromm and Andreas L. Birkenfeld
Pharmacological Reviews January 1, 2020, 72 (1) 343-379; DOI: https://doi.org/10.1124/pr.118.015735
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    • Abstract
    • I. Introduction
    • II. Solute Carrier Membrane Transport Proteins
    • III. Links to Human Metabolic Disease and Potential Targets
    • IV. Proposed Requirements for Metabolic Target Structures
    • V. Emerging Potential of Other Solute Carrier Target Structures
    • VI. Conclusion and Outlook
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